Background

In Bangladesh, bats, humans, and livestock live in close proximity, with likely overlap in consumption of common food resources (e.g., date palm sap and various fruits). Pteropus bats in Bangladesh are reservoir hosts for Nipah virus, which is transmitted from bats to people through shared consumption of date palm sap and then can be transmitted from person-to-person. Given that Nipah virus is a pathogen with pandemic potential, increased understanding of potential transmission routes is highly valuable to design prevention strategies, such as reducing opportunities for human consumption of bat contaminated fruits and date palm sap.

Objective

Hypotheses

  1. Bats visit date palm sap trees more often than fruit trees. Additionally, in villages where date palm sap is harvested, bats consume date palm sap more often than fruits. We also expect that bats visit both date palm and fruit trees more often in case villages compared to control villages.
  2. In villages where cases of Nipah virus were identified, humans and bats have more similar fruit consumption behaviors compared to villages where no Nipah cases have been identified. Observed bat visits to date palm and fruit trees (collected using camera traps) match reported bat visits from village community surveys. We also expect to find differences in animal fruit consumption between case and control villages.

Methods

Hypotheses

Hypothesis 1

  • Bats visit date palm trees more often than fruit trees.
  • Bats visit both date palm and fruit trees more often in case villages.
  • In villages where date palm sap is harvested, bats consume date palm sap more often than fruits.

Hypothesis 2

  • In villages where cases of Nipah virus were identified, humans and bats have more similar fruit consumption behaviors compared to villages where no Nipah cases have been identified.
  • Observed bat visits to date palm and fruit trees (collected using camera traps) match reported bat visits from village community surveys.
  • We also expect to find differences in animal fruit consumption between case and control villages.

Results

1. Villages observed

Begin by examining the villages included in the study. All villages have community survey information, but only villages with active date palm sap collection had camera traps at date palm trees and only villages with bats feeding at fruit trees near human fruit consumption areas had camera traps at fruit trees.

Overall, 206 villages were included in the study: 60 case, 72 near control, and 74 far control villages were included. All had community surveys completed.

  • Only 42% (86/206) of villages included in the study had active date palm sap collection.
  • More villages, 57% (118/206), had bats visiting fruit trees in areas where bats fed near to where domestic animals forage or people recently reported collecting dropped fruit.
  • Date palms observed: comparable across village types (45% case, 38% near control, 43% far control)
  • Fruit trees observed: highest for case villages (75%), followed by near control (60%), and far control (41%).

  • 32% of villages had both date palm trees and fruit trees observed, 10% only date palm trees, 25% only fruit trees, and 33% no trees
  • near control and case villages had similar percentages of villages observed, with slightly lower for far control
  • case villages had the lowest % of villages with no trees observed, while far control had the highest

  • Of the 66 villages with both tree types, only 18% received bat visits to both tree types. 74% only had visits at date palm trees, 1.5% only had visits at fruit trees, and 6% had no visits.
  • Of villages with only one tree type, it was more common for date palm trees to be visited than fruit trees.

  • When assessing across village types, case and near control villages have similar trends, with villages with both tree types seeing more visits to only date palms than visits to both tree types.

For villages with both trees observed:

  • bats make more visits per tree to date palm trees than to fruit trees
  • bat visit contamination duration is higher for date palm trees than fruit trees across villages

Few visits to fruit trees, so focusing on date palm trees:

  • longer contamination duration for Pteropus at date palm trees in villages where both date palm trees and fruit trees were observed (N = 66)
  • similar durations for non-Pteropus, but higher for pteropus in case villages

2. Date palm visits overview

As stated above, 86 (out of 206) villages had active date palm sap collection and date palm trees were subsequently observed for bat visits.

  • 162 date palm trees observed over 86 villages
  • 27 case villages, 26 near control villages, 32 far control villages

  • On average 2 date palm trees were observed per village

  • Little variation between village types for the number of date palm trees observed per village

  • Most villages with date palm trees observed had at least one tree that received a bat visit (90%)

  • A higher percentages of case and near control villages had at least one date palm tree that received a bat visit (96%) compared to far control villages (81%)
  • Overall, most date palm trees observed received at least one bat visit (79%)
  • Case villages and near control villages had a higher % of trees visited than far control

  • Because the number of visits to each tree is difficult to assess based on the visit assessment method used, visit contamination duration of each visit is used for comparison
  • While non-Pteropus bats represented a higher number of visits, the contamination duration of Pteropus visits is much longer than non-Pteropus bats
  • Cumulative contamination duration for Pteropus visits is similar across village types
  • The average contamination duration for Pteropus visits is higher in case villages, where less visits occurred but cumulative visit duration is similar

  • across village types pteropus contamination duration is higher than other bat species. This is slightly higher in case villages than control villages

Stay and contamination percentages by village type

3. Fruit tree visits overview

As stated above, 118 (out of 206) villages had fruit trees identified that were visited by bats located near the village and where animals/people consume dropped fruit, with fruit trees subsequently observed for bat visits.

  • 204 fruit trees observed over 118 villages
  • 45 case villages, 43 near control villages, 30 far control villages
  • out of 13 fruit tree types observed, only 5 had more than 2 trees observed
  • The most common tree type observed is jujube, followed by guava, star fruit, sapodilla, and banana.

  • Tree types observed at each village type are similar, with less guava trees observed at far control villages. However, less far control villages were observed overall.
  • No jujube trees were observed in case buffet villages, though this was the most common tree observed in control buffet villages

For ease of data visualization and comparisons, any trees with 1 or 2 trees observed are grouped as other. Other = fig, indian olive, betel nut, cotton tree, jack fruit, papaya, rose apple, and tamarind.

  • On average 2 trees were observed per village
##     num_tree    
##  Min.   :1.000  
##  1st Qu.:1.000  
##  Median :2.000  
##  Mean   :1.729  
##  3rd Qu.:2.000  
##  Max.   :3.000
  • Little variation between village types for the number of trees observed per village
  • Most villages with fruit trees did not have a tree that received a bat visit (24% with visits)
  • This corresponds to only 16% of overall fruit trees across villages receiving a bat visit
  • A higher percentages of far control and near control village fruit trees received bat visits than case village fruit trees

Trees that received visits by buffet and village type:

  • of the 13 tree types that were observed, 6 types received visits
  • a slightly lower percentage of trees in buffet villages received at least bat visit (12%) compared to fruit tree only villages (21%)
  • in buffet villages, the highest percentage of trees received at least one bat visit in far control villages, while in fruit only villages the highest percentage of trees received at least one bat visit in near control villages

As with date palm trees above, number of visits is a skewed reflection of the data as the same bat could be counted as multiple visits if entering and exiting the camera frame. Visit contamination durations are used.

For context, 57% of visits resulted in a contamination. Most visits to banana trees resulted in a contamination, while most visits to guava trees did not.

  • The average contamination duration for pteropus visits is higher in case and near control villages than far control villages
  • again pteropus contamination duration higher across village types (only 4 pteropus visits at far control villages, so difficult to assess)

4. Contamination durations to date palm and fruit trees conbined

  • across village types pteropus contamination duration is higher than other bat species. This is slightly higher in case villages than control villages

5. Community survey data

  • 5056 total survey responses were collected over the 206 villages
  • On average 25 surveys responses were collected per village (min-max: 12-26).
## [1] 206
## [1] 5056
##    Village_ID   participants_per_village
##  Min.   :1002   Min.   :12.00           
##  1st Qu.:1066   1st Qu.:25.00           
##  Median :2038   Median :25.00           
##  Mean   :1985   Mean   :24.54           
##  3rd Qu.:3010   3rd Qu.:25.00           
##  Max.   :3066   Max.   :26.00

Fruit survey dataset includes 206 villages and 5056 respondents. Of the 206 villages, 60 are case villages, 74 are far control, and 72 are near control. Their were 1473 respondents in case villages, 1815 from far control villages, and 1768 from near control villages. The median number of respondents per villages is 25 (min-max: 12-26).

There are four main questions that assess fruit consumption by bari members, bats, and animals separated by tree type.

  • Do members of your bari eat any [insert fruit] off the ground? (q5_frt#_5_4)
  • Do members of your bari eat any [insert fruit]? (q5_frt#_5_3)
  • Do domestic mammals (cow,sheep,goat,pig,dog,cat)eat [insert fruit] jam off ground? (q5_frt#_5_5)
  • Do bats eat any [insert fruit]? (q5_frt#_5_7)

The following questions also provide information on the trees available for bats to consume:

  • Do any fruit trees grow in or around your bari? (q5_1)
  • How many [insert fruit] trees grow in or around your bari? (q5_frt#_5_2)
Proportion of respondants reporting fruit consumption by bari members and bats and dropped fruit consumption by bari members and domestic animals (ranked by average across columns)
fruit human_fruit human_dropped_fruit animal_dropped_fruit bat_fruit average
mango 0.975 0.765 0.304 0.897 0.735
buroi 0.952 0.659 0.271 0.809 0.673
guava 0.941 0.466 0.207 0.839 0.613
banana 0.964 0.024 0.146 0.819 0.488
lichhi 0.904 0.188 0.081 0.686 0.465
betel 0.824 0.382 0.013 0.540 0.440
jackfruit 0.959 0.061 0.181 0.527 0.432
blackberry.jam 0.780 0.345 0.092 0.507 0.431
papaya 0.889 0.092 0.082 0.518 0.395
star.fruit 0.767 0.235 0.105 0.398 0.376
palmyra 0.725 0.270 0.055 0.408 0.365
indian.olive 0.790 0.241 0.068 0.335 0.359
plum 0.630 0.213 0.101 0.441 0.346
date.palm 0.614 0.214 0.077 0.438 0.336
coconut 0.880 0.170 0.004 0.068 0.281
custard.apple 0.575 0.078 0.053 0.410 0.279
sofeda 0.412 0.109 0.064 0.374 0.240
watermelon 0.840 0.006 0.046 0.044 0.234
melon 0.655 0.004 0.035 0.037 0.183
river.ebony 0.321 0.083 0.035 0.283 0.180
elephant.apple 0.442 0.077 0.036 0.138 0.173
pomegranate 0.496 0.040 0.019 0.120 0.169
wood.apple 0.388 0.063 0.009 0.042 0.125
monkey.jack 0.217 0.057 0.022 0.168 0.116
rose.apple 0.257 0.042 0.012 0.140 0.113
latkan 0.219 0.049 0.024 0.113 0.101
wild.dates 0.145 0.062 0.018 0.167 0.098
cashew.fruit 0.169 0.027 0.004 0.071 0.068
water.chestnut 0.164 0.005 0.003 0.014 0.046
rattan 0.057 0.006 0.002 0.023 0.022
uriam 0.016 0.002 0.002 0.016 0.009

Table of reported overall consumption by village type and tree type for the above questions:

Do any fruit trees grow in or around your bari?

  • The vast majority of respondents report at least 1 fruit tree growing in their bari, similar across village types.

How many [insert fruit] trees grow in or around your bari?

  • jack fruit, banana, and guava are the most common fruit trees reported in baris. About 50% of respondents report betel and buroi in their baris.

  • respondents reporting tree presence in bari is not dissimilar across buffet village types: mango, jackfruit, guava, banana, and coconut were the most commonly planted trees across baris
  • in villages with no trees observed, baris in near control villages had a high number of betel trees

Do members of your bari eat any [insert fruit] off the ground?

  • jujube/buroi is the most common fruit to be eaten off the ground. This corresponds to jujube trees making up the largest proportion of fruit trees observed for visits in this study, and guava being the second most.
  • While betel is the 3rd most commonly consumed dropped winter fruit, only 1 betel tree was observed for fruit visits
  • generally little variation between village types

Do members of your bari eat any [insert fruit]?

  • high winter fruit consumption, similar between village types

Do domestic mammals (cow,sheep,goat,pig,dog,cat) eat [insert fruit] off ground?

  • Again jujube/buroi ang guava consumption is highest
  • Again, similar across village types

Do bats eat any [insert fruit]?

  • Highest reported bat consumption of winter fruits for guava, banana, and jujube/buroi (~80%).
  • matches these three tree types all receiving bat visits

Reported consumption of dropped fruits by bari members was highest for mango (76%), buroi (66%), guava (47%), and betel (38%). Consumption was lowest for melon (0%), water chestnut (0%), and uriam (0%). While reported dropped fruit consumption of date palm fruit was comparatively lower, at (21%), dropped date palm fruit consumption was highest among case villages by the largest difference of any fruit. Case village consumption of date palm fruit was reported to be 29%, control near 21%, and control far 16%. The average reported consumption among all fruits was 16%.

Reported consumption of fruits by bari members among fruit tree types was generally high (mean = 57%) with little difference in consumption between village types. Fruits consumed the most were mango (98%), jackfruit (96%), banana (96%), buroi (95%), and guava (94%). However, date palm fruit consumption was again highest among case villages by the largest difference of any fruit. Case village consumption of date palm fruit was reported to be 71%, control near 62%, and control far 52%.

Reported consumption of dropped fruits by domestic animals was much lower than human consumption (mean = 7%). Dropped fruit consumption was highest for mango (30%), buroi (27%), guava (21%), jackfruit (18%), and banana (15%). Date palm fruit consumption was 8% overall; 7% in case villages, 6% in near control villages, and 10% in far control villages. Difference in consumption between village types overall seems to vary more among domestic animals than humans, though this may be due to decreased accuracy in observations of animal fruit consumption compared to human fruit consumption.

Reported consumption of fruits by bats was on average 33%. This was highest for mango (90%), guava (84%), buroi (81%), and banana (82%). In each case consumption was slightly higher in case villages compared to near control villages, and higher in near control villages than far control villages. Date palm fruit consumption was 44% overall; 52% in case villages, 40% in near control villages, and 40% in far control villages.

Date palm fruit consumption was highest in case villages for bat fruit consumption, human fruit consumption, and human dropped fruit consumption. Dropped fruit consumption is a proxy for consumption of fruits that may have been bitten or contaminated by bats. However, the high reported consumption of mango, guava, and buroi by bats compared with high dropped fruit consumption of these fruits by humans and animals is potentially notable.

Of the tree types included on the survey, only 6 had visits recorded using camera traps.

  • bat reported fruit consumption and human reported fruit consumption are similar for each tree type
  • there is little consumption variation between village types. However, consumption is slightly higher in case and near control villages than far control for guava, banan, and jujube/buroi.
  • Banana, jujube/buroi, and guava had the higest reported bat consumption and a high proportion of observed trees that received at least one visit. Potential source of food contamination overlap.

When examining bat fruit consumption more closely, for the 6 tree types that received bat visits, there is some mild difference in village types.

  • for banana, buroi, and guava, consumption is slightly higher in case and near control villages than far control villages
  • for date palm, consumption is higher in case villages than control villages
# plot bat fruit consumption with x-axis ranked by the average
rank_b_fruit_grouped_mean %>%
  filter(fruit == "banana" | fruit == "date.palm"| fruit == "star.fruit"| fruit == "sofeda" | fruit == "guava" | fruit == "buroi") %>% 
  ggplot(aes(x = fruit, y = bat_fruit, color = case_control_group)) +
  geom_jitter(height = 0, width = 0.2, alpha = 0.8) +
  labs(x = "Fruit type",
       y = "Proportion of baris with bats\nconsuming fruit",
       title = "Proportion of respondants reporting bat consumption\nof fruits by village type") +
  theme_bw() +
  theme(axis.text.x = element_text(angle = 45, hjust = 1),
        axis.title.y = element_text(vjust = 1)) +
  scale_color_manual(
    name = "Village type",
    values = c(
      "case" = "#E69F00",
      "control, far" = "#56B4E9",
      "control, near" = "#009E73"
    )
  )

Additional survey questions

There are several survey questions that provide additional insight into fruit consumption of humans, bats, and animals.

Human fruit consumption questions:

Reported frequency of dropped fruit consumption by bari members
case_control_group median_household mean_household count numNA response_rate sum_1 prop_1 sum_2 prop_2 sum_3 prop_3
case 3 2.736 546 927 0.371 53 0.097 38 0.070 455 0.833
control, far 3 2.735 950 865 0.523 98 0.103 56 0.059 796 0.838
control, near 3 2.694 886 882 0.501 109 0.123 53 0.060 724 0.817

Reported dropped fruit consumption by bari members was lowest in case villages, at 42%, compared to both categories of control villages. Of those who reported dropped fruit consumption, most stated only occasional consumption.

Domestic animals fruit consumption questions:

Proportion of respondants reporting feeding dropped fruit consumption to domestic animals in bari
case_control_group count numNA response_rate sum_households proportion_households
case 1298 175 0.881 290 0.223
control, far 1431 384 0.788 497 0.347
control, near 1539 229 0.870 473 0.307
Proportion of respondants reporting dropped fruit consumption by domestic animals in bari
case_control_group count numNA response_rate sum_households proportion_households
case 1298 175 0.881 189 0.146
control, far 1431 384 0.788 289 0.202
control, near 1539 229 0.870 364 0.237 
## <labelled<double>[4]>: How often do you feed bat or bird bitten fruit to your domestic animals?
## [1] NA  2  3  1
## 
## Labels:
##  value                label
##      1            Most days
##      2 Once or twice a week
##      3    Only occasionally
Reported frequency of bari members feeding dropped fruit to domestic animals
case_control_group median_household mean_household count numNA response_rate sum_1 prop_1 sum_2 prop_2 sum_3 prop_3
case 3 2.725 189 1284 0.128 19 0.101 14 0.074 156 0.825
control, far 3 2.830 289 1526 0.159 14 0.048 21 0.073 254 0.879
control, near 3 2.734 364 1404 0.206 37 0.102 23 0.063 304 0.835
Proportion of respondants reporting feeding raw date palm sap to domestic animals in bari
case_control_group count numNA response_rate sum_households proportion_households
case 58 1415 0.039 13 0.224
control, far 99 1716 0.055 7 0.071
control, near 49 1719 0.028 14 0.286
Proportion of respondants reporting feeding dirty raw date palm sap to domestic animals in bari
case_control_group count numNA response_rate sum_households proportion_households
case 27 1446 0.018 9 0.333
control, far 31 1784 0.017 8 0.258
control, near 18 1750 0.010 9 0.500
Reported frequency of bari members feeding date palm sap to domestic animals
case_control_group median_household mean_household count numNA response_rate sum_1 prop_1 sum_2 prop_2 sum_3 prop_3 sum_4 prop_4
case 2 2.222 9 1464 0.006 3 0.333 3 0.333 1 0.111 2 0.222
control, far 2 2.375 8 1807 0.004 0 0.000 6 0.750 1 0.125 1 0.125
control, near 3 2.778 9 1759 0.005 0 0.000 4 0.444 3 0.333 2 0.222
Proportion of respondants reporting other people in the village feeding dirty raw date palm sap to domestic animals in their bari
case_control_group count numNA response_rate sum_households proportion_households
case 1471 2 0.999 224 0.152
control, far 1814 1 0.999 259 0.143
control, near 1768 0 1.000 197 0.111

Consumption of fruits on the ground by animals 30%, and is lowest in case villages at 22%. Feeding bat or bird bitten fruits to domestic animals is less common (20%), but is again lowest in case villages at 15%. Among those who reported feeding these to domestic animals the behavior was reported to be most often done only occasionally in all village types.

Interestingly, more respondents reported that raw date palm sap and dirty sap is fed to domestic animals in near control villages compared to far control or case villages. However, in far control and case villages date palm sap is fed to animals most often daily compared to about once per week in near control villages.

An important thing to note, however, is that response rate for some of these questions is much lower than the questions about fruit trees. For example, question q3_12 about feeding sap to animals had a response rate of only 0.44%.

Bat fruit consumption questions:

Proportion of respondants reporting bird or bat bitten fruit on the ground in their bari
case_control_group count numNA response_rate sum_households proportion_households
case 1470 3 0.998 1298 0.883
control, far 1810 5 0.997 1431 0.791
control, near 1767 1 0.999 1540 0.872
Proportion of respondants reporting bird or bat bitten fruit on the ground in their bari during this time of year (winter)
case_control_group count numNA response_rate sum_households proportion_households
case 1298 175 0.881 928 0.715
control, far 1431 384 0.788 733 0.512
control, near 1540 228 0.871 902 0.586
Proportion of respondants reporting seeing large fruit bats in their fruit trees at night
case_control_group count numNA response_rate sum_households proportion_households
case 1470 3 0.998 631 0.429
control, far 1805 10 0.994 954 0.529
control, near 1767 1 0.999 923 0.522
Reported frequency of bari members reporting bats in their fruit trees at night
group mean_household count numNA response_rate sum_1 prop_1 sum_2 prop_2 sum_3 prop_3 sum_4 prop_4
1 67.651 923 845 0.522 156 0.169 51 0.055 380 0.412 276 0.299
2 207.295 954 861 0.526 189 0.198 60 0.063 390 0.409 119 0.125
3 24.843 631 842 0.428 124 0.197 67 0.106 272 0.431 154 0.244

Villagers report commonly seeing dropped fruits that have been bitten by bats or birds. This is highest in case villages at 88%, followed by near controls at 87%, and far controls at 79%.

Of those who reported that they see fruits on the ground that have been bitten by bats or birds, about 60% reported that it occurs during this time of year (winter). This was highest in case villages, at 71%, followed by near controls at 58% and far controls at 51%.

Case villagers reported seeing fruit bats in their trees at night the least, at 43%, compared to control villages, both at 52%.

Other information

Number of trees in bari (q5_frt#_5_2)

Animal ownership (q4_#_1)

Discussion

Hypothesis 1

  • Bats visit date palm sap trees more often than fruit trees. –> yes
  • Bats visit both date palm and fruit trees more often in case villages. –> yes, measured by visit contamination duration
  • In villages where date palm sap is harvested, bats consume date palm sap more often than fruits. –> yes

Hypothesis 2

  • In villages where cases of Nipah virus were identified, humans and bats have more similar fruit consumption behaviors compared to villages where no Nipah cases have been identified.
  • Observed bat visits to date palm and fruit trees (collected using camera traps) match reported bat visits from village community surveys.
  • We also expect to find differences in animal fruit consumption between case and control villages.